An open-pollinated design for mapping imprinting genes in natural populations

With the increasing recognition of its role in trait and disease development, it is crucial to account for genetic imprinting to illustrate the genetic architecture of complex traits. Genetic mapping can be innovated to test and estimate effects of genetic imprinting in a segregating population derived from experimental crosses. Here, we describe and assess a design for imprinting detection in natural plant populations. This design is to sample maternal plants at random from a natural population and collect open-pollinated (OP) seeds randomly from each maternal plant and germinate them into seedlings. A two-stage hierarchical platform is constructed to jointly analyze maternal and OP progeny markers. Through tracing the segregation and transmission of alleles from the parental to progeny generation, this platform allows parent-of-origin-dependent gene expression to be discerned, providing an avenue to estimate the effect of imprinting genes on a quantitative trait. The design is derived to estimate imprinting effects expressed at the haplotype level. Its usefulness and utilization were validated through computer simulation. This OP-based design provides a tool to detect the genomic distribution and pattern of imprinting genes as an important component of heritable variation that is neglected in traditional genetic studies of complex traits.

[1]  J. Rafalski,et al.  Association genetics in crop improvement. , 2010, Current opinion in plant biology.

[2]  Rongling Wu,et al.  Computing genetic imprinting expressed by haplotypes. , 2009, Methods in molecular biology.

[3]  Arturas Petronis,et al.  The Analysis of Parental Origin of Alleles May Detect Susceptibility Loci for Complex Disorders , 1999, Human Heredity.

[4]  Pardis C Sabeti,et al.  Linkage disequilibrium in the human genome , 2001, Nature.

[5]  Rongling Wu,et al.  A model for family-based case-control studies of genetic imprinting and epistasis , 2013, Briefings Bioinform..

[6]  Rongling Wu,et al.  The case for molecular mapping in forest tree breeding. , 2010 .

[7]  Rongling Wu,et al.  A General Framework for Statistical Linkage Analysis in Multivalent Tetraploids , 2005, Genetics.

[8]  Ming Luo,et al.  A Genome-Wide Survey of Imprinted Genes in Rice Seeds Reveals Imprinting Primarily Occurs in the Endosperm , 2011, PLoS genetics.

[9]  Rongling Wu,et al.  A Model for Transgenerational Imprinting Variation in Complex Traits , 2010, PloS one.

[10]  Rongling Wu,et al.  Simultaneous maximum likelihood estimation of linkage and linkage phases in outcrossing species. , 2002, Theoretical population biology.

[11]  Rongling Wu,et al.  Algorithms for Molecular Biology , 2009 .

[12]  M. Surani,et al.  Role of paternal and maternal genomes in mouse development , 1984, Nature.

[13]  B. Cattanach,et al.  Differential activity of maternally and paternally derived chromosome regions in mice , 1985, Nature.

[14]  Jian Zhang,et al.  A quantitative genetic and epigenetic model of complex traits , 2012, BMC Bioinformatics.

[15]  Rongling Wu,et al.  A multilocus likelihood approach to joint modeling of linkage, parental diplotype and gene order in a full-sib family , 2004, BMC Genetics.

[16]  B. Tycko,et al.  Physiological functions of imprinted genes , 2002, Journal of cellular physiology.

[17]  Henk Bovenhuis,et al.  On the detection of imprinted quantitative trait loci in experimental crosses of outbred species. , 2002, Genetics.

[18]  J W Gray,et al.  NOEY2 (ARHI), an imprinted putative tumor suppressor gene in ovarian and breast carcinomas. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[19]  G. Casella,et al.  Sequencing Complex Diseases With HapMap , 2004, Genetics.

[20]  J. Johnson,et al.  Sequencing drug response with HapMap , 2005, The Pharmacogenomics Journal.

[21]  Rongling Wu,et al.  Modeling Haplotype-Haplotype Interactions in Case-Control Genetic Association Studies , 2012, Front. Gene..

[22]  Rongling Wu,et al.  Multilocus genomics of outcrossing plant populations. , 2009, Theoretical population biology.

[23]  R. Jirtle,et al.  Genomic imprinting: implications for human disease. , 1999, The American journal of pathology.

[24]  J. Cheverud,et al.  Genomic imprinting and parent-of-origin effects on complex traits , 2013, Nature Reviews Genetics.

[25]  G. Casella,et al.  Joint linkage and linkage disequilibrium mapping of quantitative trait loci in natural populations. , 2002, Genetics.

[26]  Rongling Wu,et al.  A computational framework for the inheritance pattern of genomic imprinting for complex traits , 2012, Briefings Bioinform..

[27]  Patrick S. Schnable,et al.  Parent-of-Origin Effects on Gene Expression and DNA Methylation in the Maize Endosperm[W] , 2011, Plant Cell.

[28]  Célia Baroux,et al.  Regulation and Flexibility of Genomic Imprinting during Seed Development[W] , 2011, Plant Cell.

[29]  W Davies,et al.  Multiple marker mapping of quantitative trait loci in a cross between outbred wild boar and large white pigs. , 1998, Genetics.

[30]  A. Ferguson-Smith.  Genomic imprinting: the emergence of an epigenetic paradigm , 2011, Nature Reviews Genetics.

[31]  Z B Zeng,et al.  Joint linkage and linkage disequilibrium mapping in natural populations. , 2001, Genetics.

[32]  W. Reik,et al.  Genomic imprinting: parental influence on the genome , 2001, Nature Reviews Genetics.

[33]  Zhiwu Zhang,et al.  Association Mapping: Critical Considerations Shift from Genotyping to Experimental Design , 2009, The Plant Cell Online.

[34]  Rongling Wu,et al.  An algorithmic model for constructing a linkage and linkage disequilibrium map in outcrossing plant populations. , 2009, Genetics research.

[35]  R. Martienssen,et al.  Reprogramming of DNA Methylation in Pollen Guides Epigenetic Inheritance via Small RNA , 2012, Cell.

[36]  Rongling Wu,et al.  Model for mapping imprinted quantitative trait loci in an inbred F2 design. , 2006, Genomics.

[37]  H. Spencer,et al.  A census of mammalian imprinting. , 2005, Trends in genetics : TIG.

[38]  Wu Rongling,et al.  A multilocus model for constructing a linkage disequilibrium map in human populations. , 2009 .

[39]  D. Botstein,et al.  Genome-wide scan of bipolar disorder in 65 pedigrees: supportive evidence for linkage at 8q24, 18q22, 4q32, 2p12, and 13q12 , 2003, Molecular Psychiatry.

[40]  Wei Hou,et al.  Modeling sequence-sequence interactions for drug response , 2007, Bioinform..

[41]  Rongling Wu,et al.  A General Quantitative Genetic Model for Haplotyping a Complex Trait in Humans , 2007, Current genomics.

[42]  Rongling Wu,et al.  A random model for mapping imprinted quantitative trait loci in a structured pedigree: an implication for mapping canine hip dysplasia. , 2007, Genomics.

[43]  R. Sederoff,et al.  Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. , 1994, Genetics.

[44]  Bing Wang,et al.  Genomic imprinting effects on adult body composition in mice , 2008, Proceedings of the National Academy of Sciences.

[45]  Rongling Wu,et al.  A Statistical Model for Estimating Maternal-Zygotic Interactions and Parent-of-Origin Effects of QTLs for Seed Development , 2008, PloS one.

[46]  Rongling Wu,et al.  A Statistical Design for Testing Transgenerational Genomic Imprinting in Natural Human Populations , 2011, PloS one.

[47]  D. de Koning,et al.  Genome Scan for Parent-of-Origin QTL Effects on Bovine Growth and Carcass Traits , 2011, Front. Gene..

[48]  Jean-Marcel Ribaut,et al.  Joint linkage–linkage disequilibrium mapping is a powerful approach to detecting quantitative trait loci underlying drought tolerance in maize , 2010, Proceedings of the National Academy of Sciences.

[49]  Peter H. Westfall,et al.  Testing Association of Statistically Inferred Haplotypes with Discrete and Continuous Traits in Samples of Unrelated Individuals , 2002, Human Heredity.

[50]  Rongling Wu,et al.  A case-control design for testing and estimating epigenetic effects on complex diseases , 2014, Briefings Bioinform..